Abstract
Crop productivity is strictly related to genome stability, an essential requisite for optimal plant growth/development. Genotoxic agents (e.g., chemical agents, radiations) can cause both chemical and structural damage to DNA. In some cases, they severely affect the integrity of plant genome by inducing base oxidation, which interferes with the basal processes of replication and transcription, eventually leading to cell death. The cell response to oxidative stress includes several DNA repair pathways, which are activated to remove the damaged bases and other lesions. Information concerning DNA repair in plants is still limited, although results from gene profiling and mutant analysis suggest possible differences in repair mechanisms between plants and other eukaryotes. The present review focuses on the base- and nucleotide excision repair (BER, NER) pathways, which operate according to the most common DNA repair rule (excision of damaged bases and replacement by the correct nucleotide), highlighting the most recent findings in plants. An update on DNA repair in organelles, chloroplasts and mitochondria is also provided. Finally, it is generally acknowledged that DNA repair plays a critical role during seed imbibition, preserving seed vigor. Despite this, only a limited number of studies, described here, dedicated to seeds are currently available.
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Abbreviations
- At:
-
Arabidopsis thaliana
- BER:
-
Base excision repair
- 8-oxo-dG:
-
7, 8-Dihydro-8-oxoguanine
- DR:
-
Direct repair
- DSBR:
-
Double-strand break repair
- GGR:
-
Global genome repair
- HR:
-
Homologous recombination
- MMR:
-
Mismatch repair
- Mt:
-
Medicago truncatula
- NER:
-
Nucleotide excision repair
- NHEJ:
-
Nonhomologous end joining
- PEG:
-
Polyethylene glycol
- QRT-PCR:
-
Quantitative real-time polymerase chain reaction
- ROS:
-
Reactive oxygen species
- TCR:
-
Transcription coupled repair
- Tdp:
-
Tyrosyl-DNA phosphodiesterase
- TFIIS:
-
Transcription elongation factor II-S
- top1:
-
Gene encoding DNA topoisomerase I
- topo I:
-
DNA topoisomerase I
References
Alseth I, Korvald H, Osman F, Seeberg E, Bioras M (2004) A general role of the DNA glycosylase Nth1 in the abasic sites cleavage step of base excision repair in Schizosaccharomyces pombe. Nucleic Acids Res 32:5119–5125
Amor Y, Babiychuk E, Inze D, Levine A (1998) The involvement of poly(ADP-ribose) polymerase in the oxidative stress response in plants. FEBS Lett 440:1–7
Balestrazzi A, Chini A, Bernacchia G, Bracci A, Luccarini G, Cella R, Carbonera D (2000) Carrot cells contain two top1 genes having the coding capacity for two distinct DNA topoisomerases I. J Exp Bot 51:1979–1990
Balestrazzi A, Locato V, Bottone MG, De Gara L, Biggiogera M, Pellicciari C, Botti S, Di Gesù D, Donà M, Carbonera D (2010a) Response to UV-C radiation in topo I-deficient carrot cells with low ascorbate levels. J Exp Bot 61:575–585
Balestrazzi A, Confalonieri M, Macovei A, Carbonera D (2010b) Seed imbibition in Medicago truncatula Gaertn.: expression profiles of DNA repair genes in relation to PEG-mediated stress. J Plant Physiol. doi:10.1016/j.jplph.2010.10.008
Boesch P, Ibrahim N, Paulus F, Cosset A, Tarasenko V, Dietrich A (2009) Plant mitochondria possess a short-patch base excision DNA repair pathway. Nucleic Acids Res 37:5690–5700
Boesch P, Weber-Lofti F, Ibrahim N, Tarasenko V, Cosset A, Paulus F, Lightowlers RN, Dietrich A (2010) DNA repair in organelles: pathways, organization, regulation, relevance in disease and aging. Biochim Bioph Acta. doi:10.1016/j.bbamcr.2010.10.002
Booth V, Koth CM, Edwards AM, Arrowsmith CH (2000) Structure of a conserved domain common to the transcription factors TFIIS, elongin A and CRSP70. J Biol Chem 275:31266–31268
Brown JA, Pack LR, Sanman LE, Suo Z (2010) Efficiency and fidelity of human DNA polymerases λ and β during gap-filling DNA synthesis. DNA Repair. doi:10.1016/j.dnarep.2010.09.005
Butler LH, Hay FR, Ellis RH, Smith RD, Murray TB (2009) Priming and re-drying improves the survival of mature seeds of Digitalis purpurea during storage. Ann Bot 103:1261–1270
Caldecott KW (2001) Mammalian DNA single-strand break repair: an X-ra(y)ted affair. Bioessays 23:447–455
Conconi A, Bespalov VA, Smerdon MJ (2002) Transcription-coupled repair in RNA polymerase I-transcribed genes of yeast. Proc Natl Acad Sci USA 99:649–654
Cordoba-Canero D, Dubois E, Ariza RR, Doutriaux M-P, Roldan-Arjona T (2009a) Arabidopsis uracil DNA glycosylase (UNG) is required for base excision repair of uracil and increases plant sensitivity to 5-fluorouracil. J Biol Chem 285:7475–7483
Cordoba-Canero D, Morales-Ruiz T, Roldan-Arjona T, Ariza RR (2009b) Single-nucleotide and long-patch base excision repair of DNA damage in plants. The Plant J 60:716–728
Costa RM, Morgante PG, Berra CM, Nakabashi M, Bruneau D, Bouchez D, Sweder KS, Van Sluys MA, Menck CF (2001) The participation of AtXPB1, the XPB/RAD25 homologue gene from Arabidopsis thaliana, in DNA repair and plant development. Plant J 28:385–395
Cox MM (2007) Regulation of bacterial RecA protein function. Crit Rev Biochem Mol Biol 42:41–63
Dany AL, Tisser A (2001) A functional OGG1 homologue from Arabidopsis thaliana. Mol Gen Genom 265:293–301
Davies H, Probert R (2004) Protocol for comparative seed longevity testing sheet. Royal Botanic Gardens, Kew. http:\\www.kew.org/msbp/scitech/publications/comparativelongevity.pdf.London
Doucet-Chabeaud G, Godon C, Brutesco C, de Murcia G, Kazmaier M (2001) Ionizing radiation induces the expression of PARP-1 and PARP-2 genes in Arabidopsis. Mol Gen Genom 265:954–963
Dubest S, Gallego ME, White CI (2002) Role of the AtRad1p endonuclease in homologous recombination in plants. EMBO Rep 3:1049–1054
El-Khamisy SF, Saifi GM, Weinfeld M, Johansson F, Helleday T, Lupski JR, Caldecott KW (2005) Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy. Nature 434:108–113
Fortini P, Dogliotti E (2007) Base damage and single-strand break repair: mechanisms and functional significance of short- and long-patch repair subpathways. DNA Repair (Amst) 6:398–409
Friedberg EC (1996) Relationships between DNA repair and transcription. Annu Rev Biochem 65:15–42
Garcia-Ortiz MV, Ariza R, Roldan-Arjona T (2001) An OGG1 orthologue encoding a functional 8-oxoguanine DNA glycosylase/lyase in Arabidopsis thaliana. Plant Mol Biol 47:795–804
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Grasser M, Kane CM, Merkle T, Melzer M, Emmersen J, Grasser KD (2009) Transcription elongation factor TFIIS is involved in Arabidopsis seed dormancy. J Mol Biol 386:598–611
Gutman BL, Niyogi KN (2009) Evidence for base excision repair of oxidative DNA damage in chloroplasts of Arabidopsis thaliana. J Biol Chem 284:17006–17012
Hunt L, Holdsworth MJ, Gray JE (2007) Nicotinamidase activity is important for germination. Plant J 51:341–351
Inamdar KV, Pouliot JJ, Zhou T, Lees-Miller SP, Rasouli-Nia A, Povirk LF (2002) Conversion of phosphoglycolate to phosphate termini on 3′-overhangs of DNA double strand breaks by the human tyrosyl-DNA phosphodiesterase hTdp1. J Biol Chem 277:27162–27168
Jiang CZ, Yee J, Mitchell DL, Britt AB (1997) Photorepair mutants of Arabidopsis. Proc Natl Acad Sci USA 94:7441–7445
Kaiser G, Kleiner O, Beisswenger C, Batschauer A (2009) Increased DNA repair in Arabidopsis plants overexpressing CPD photolyase. Planta 230:505–515
Kimura S, Sakaguchi K (2006) DNA repair in plants. Chem Rev 106:753–766
Kranner I, Minibayeva FV, Beckett RP, Seal CE (2010) What is stress? Concepts, definitions and applications in seed science. New Phytol. doi:10.1111/j.1469-8137.2010.03461.x
Kunz BA, Anderson HJ, Osmond MJ, Vonarx EJ (2005) Components of nucleotide excision repair and DNA damage tolerance in Arabidopsis thaliana. Environ Mol Mutat 45:115–127
Kuraoka I, Suziki K, Ito S, Hayashida M, Kwei JS, Ikegami T, Handa H, Nakabeppu T, Tanaka K (2007) RNA polymerase II bypasses 8-oxoguanine in the presence of transcription factor TFIIS. DNA Repair 6:841–851
Lebedeva N, Rachkunova N, Boiteux S, Lavrik O (2008) Trapping of human DNA topoisomerase I by DNA structures mimicking intermediates of DNA repair. IUBMB Life 60:130–134
Lee S-Y, Kim H, Hwang H-J, Jeong Y-M, Na Y-M, Woo J-C, Kim S-G (2010) Identification of tyrosyl-DNA phosphodiesterase as a novel DNA damage repair enzyme in Arabidopsis. Plant Physiol. doi:10.1104/pp.110.165068
Liu Z, Hong SW, Escobar M, Vierling E, Mitchell DL, Mount DW, Hall JD (2003) Arabidopsis UVH6, a homolog of human XPD and yeast RAD3 DNA repair genes, functions in DNA repair and is essential for plant growth. Plant Physiol 132:1405–1414
Liu L, Lee J, Zhou P (2010) Navigating the nucleotide excision repair threshold. J Cell Physiol 224:585–589
Macovei A, Balestrazzi A, Confalonieri M, Carbonera D (2010a) The Tdp1 (tyrosyl-DNA phosphodiesterase) gene family in barrel medic (Medicago truncatula Gaertn.): bioinformatic investigation and expression profiles in response to copper- and PEG-mediated stress. Planta 232:393–407
Macovei A, Balestrazzi A, Confalonieri M, Buttafava A, Carbonera D (2010b) The TFIIS and TFIIS-like genes from Medicago truncatula are involved in oxidative stress response. Gene. doi:10.1016/j.gene.2010.09.004
Mielke C, Kalfalah FM, Christensen MO, Boege F (2007) Rapid and prolonged stalling of human DNA topoisomerase I in UVA-irradiated genomic areas. DNA Repair 6:1757–1763
Molinier J, Lechner E, Dumbliariskas E, Genschik P (2008) Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. PLoS Genet 4:e1000093
Murphy TM, George A (2005) A comparison of two DNA base excision repair glycosylases from Arabidopsis thaliana. Biochem Biophys Res Commun 329:869–872
Murphy TM, Belmonte M, Shu S, Britt AB, Hatteroth J (2009) Requirement for abasic endonuclease gene homologues in Arabidopsis seed development. PLoS ONE 4:e4297
Nielsen BL, Cupp JD, Brammer J (2010) Mechanisms for maintenance, replication and repair of the chloroplast genome in plants. J Exp Bot 61:2535–2537
Puchta H, Hohn B (1996) From centimorgans to base pairs: homologous recombination in plants. Trends Plant Sci 1:340–348
Rajjou L, Debeaujon I (2008) Seed longevity: survival and maintenance of high germination ability of dry seeds. C R Biol 331:796–805
Rizhsky L, Liang H, Mittler R (2002) The combined effects of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151
Roldan-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681:169–179
Rowan BA, Oldenburg DJ, Bendich AJ (2010) RecA maintains the integrity of chloroplast DNA molecules in Arabidopsis. J Exp Bot 61:2575–2588
Sanan-Mishra N, Pham XH, Sopory SK, Tuteja N (2005) Pea DNA helicase 45 overexpression in tobacco confers high salinity tolerance without affecting yield. Proc Natl Acad Sci USA 102:509–514
Seki M, Ayako K, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biotech 14:194–199
Shedge V, Arrieta-Montel M, Christensen AC, Mackenzie SA (2007) Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19:1251–1264
Shuck SC, Short EA, Turchi JJ (2008) Eukaryotic nucleotide excision repair: from understanding mechanisms to influencing biology. Cell Res 18:64–72
Singh SK, Roy S, Roy Choudhury S, Sengupta M (2010) DNA repair and recombination in higher plants: insights from comparative genomics of Arabidopsis and rice. BMC Genomics 11:443
Stivers JT, Jiang YL (2003) A mechanistic perspective on the chemistry of DNA repair glycosylases. Chem Rev 103:2729–2759
Svejstrup JQ (2007) Contending with transcriptional arrest during RNAPII transcription elongation. Trends Biochem Sci 32:165–171
Tanaka A, Sakamoto A, Ishigaki Y, Nikaido O, Sun G, Hase Y, Shikazono N, Tano S, Watanabe H (2002) An ultraviolet-B-resistant mutant with enhanced DNA repair in Arabidopsis. Plant Physiol 129:64–71
Taylor RM, Hamer MJ, Rosamond J, Bray CM (1998) Molecular cloning and functional analysis of the Arabidopsis thaliana DNA ligase I homologue. Plant J 14:75–81
Tester M, Bacic A (2005) Abiotic stress tolerance in grasses from model plants to crop plants. Plant Physiol 137:791–793
Tomkinson AE, Mackey ZB (1998) Structure and function of mammalian ligases. Mutat Res/DNA Repair 407:1–9
Tuteja N (2003) Plant DNA helicases: the long unwinding road. J Exp Bot 54:2201–2214
Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. Mutat Res 681:134–149
Uchiyama Y, Suzuki Y, Sakaguchi K (2008) Characterization of plant XRCC1 and its interaction with proliferating cell nuclear antigen. Planta 227:1233–1241
Vanderauwera S, de Block M, Van de Steene N, van de Cotte B, Metzlaff M, Van Breusegem F (2007) Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci USA 104:15150–15155
Vashisht AA, Tuteja N (2006) Stress responsive DEAD-box helicases: a new pathway to engineer plant stress tolerance. J Photochem Photobiol B Biol 84:150–160
Veselova TV, Veselovskii VA, Usmanov PD, Usmanova OV, Kozar VI (2003) Hypoxia and imbibition injuries to aging seeds. Russian J Plant Physiol 50:835–842
Volker M, Mone MJ, Karmakar P, van Hoffen A, Schul W, Vermeulen W, Hoeijmakers JH, van Driel R, van Zeeland AA, Mullenders LH (2001) Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell 8:213–224
Wang H, Zhai L, Xu J, Joo HY, Jackson S, Erdjument-Bromage H, Tempst P, Xiong Y, Zhang Y (2006) Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular responses to DNA damage. Mol Cell 22:383–394
Waterworth WM, Kozak J, Provost CM, Bray CM, Angelis KJ, West CE (2009) DNA ligase 1 deficient plants display severe growth defects and delayed repair of both DNA single and double strand breaks. BCM Plant Biol 9:79
Waterworth WM, Masnavi G, Bhardwaj RM, Jiang Q, Bray CM, West CE (2010) A plant DNA ligase is an important determinant of seed longevity. Plant J. doi:10.1111/j.1365-313X.2010.04285.x
Wu X, Li J, Li X, Hsieh CL, Burgers PM, Lieber MR (1996) Processing of branched DNA intermediates by a complex of human FEN-1 and PCNA. Nucleic Acids Res 24:2036–2043
Yasukawa T, Sugimura K, Fukuda M, Yamazaki K, Katajina O, Okumura K, Aso T (2007) Functional characterization of a mammalian transcription factor, elongin A. Biochem Biophys Res Commun 352:237–243
Zharkov DO (2008) Base excision DNA repair. Cell Mol Life Sci 65:1544–1565
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This research was supported by Fondo di Ateneo per la Ricerca, University of Pavia.
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Communicated by R. Reski.
A contribution to the Special Issue: Plant Biotechnology in Support of the Millennium Development Goals.
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Balestrazzi, A., Confalonieri, M., Macovei, A. et al. Genotoxic stress and DNA repair in plants: emerging functions and tools for improving crop productivity. Plant Cell Rep 30, 287–295 (2011). https://doi.org/10.1007/s00299-010-0975-9
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DOI: https://doi.org/10.1007/s00299-010-0975-9